Andrew Edward Z. Short

Phylogeny and evolution of Staphyliniformia and Scarabaeiformia: forest litter as a stepping stone for diversification of nonphytophagous beetles

The beetle series Staphyliniformia exhibits extraordinary taxonomic, ecological and morphological diversity. To gain further insight into staphyliniform relationships and evolution, we reconstructed the phylogeny of Staphyliniformia using DNA sequences from nuclear 28S rDNA and the nuclear protein‐coding gene CAD for 282 species representing all living families and most subfamilies, a representative sample of Scarabaeiformia serving as a near outgroup, and three additional beetles as more distant outgroups. Under both Bayesian inference (BI) and maximum likelihood inference (MLI), the major taxa within Staphyliniformia are each monophyletic: (i) Staphylinoidea, (ii) Hydrophiloidea s.l., and the contained superfamilies (iii) Hydrophiloidea s.s. and (iv) Histeroidea, although Staphylinoidea and Hydrophiloidea s.l. are not strongly supported by MLI bootstrap. Scarabaeiformia is monophyletic under both methods of phylogenetic inference. However, the relative relationships of Staphylinoidea, Hydrophiloidea s.l. and Scarabaeiformia differ between BI and MLI: under BI, Staphyliniformia and Scarabaeiformia were sister groups; under MLI, Hydrophiloidea s.l. and Scarabaeiformia were sister groups and these together were sister to Staphylinoidea. The internal relationships in Scarabaeiformia were similar under both methods of phylogenetic inference, with Cetoniinae, Dynastinae + Rutelinae, Hybosoridae, Passalidae, Scarabaeidae and Scarabaeinae recovered as monophyla. Histeridae comprised two major clades: (1) Abraeinae, Trypanaeine and Trypeticinae; and (2) Chlamydopsinae, Dendrophilinae, Haeteriinae, Histerinae, Onthophilinae, Saprininae and Tribalinae. The relationships among early‐divergent Hydrophiloidea differed between BI and MLI, and overall were unresolved or received only moderate to low nodal support. The staphylinoid families Agyrtidae, Hydraenidae and Ptiliidae were recovered as monophyletic; the latter two were sister taxa, and Staphylinidae + Silphidae was also monophyletic. Silphidae was placed within Staphylinidae in close relation to a subset of Tachyporinae. Pselaphinae and Scydmaeninae were both recovered within Staphylinidae, in accordance with recent analyses of morphological characters, although not always with recently proposed sister taxa. None of the four major groups of Staphylinidae proposed by Lawrence and Newton (1982) was recovered as monophyletic. Certain highly specialized staphyliniform habits and morphologies, such as abdominal defensive glands and reduced elytra, have arisen in parallel in separate lineages. Further, our analyses support two major transitions to an aquatic lifestyle within Staphyliniformia: once within Staphylinoidea (Hydraenidae), and once within Hydrophiloidea s.l. (Hydrophiloidea s.s.). On a smaller scale, the most common transition is from litter to subcortical or to periaquatic microhabitats and the next most common is from litter to carrion and to fungi. Overall, transitions to periaquatic microhabitats were the most numerous. The broad picture in Staphyliniformia seems to be a high level of evolutionary plasticity, with multiple possible pathways to and from many microhabitat associations, and litter as a major source microhabitat for diversification. In Scarabaeiformia, the most common transitions were from litter to foliage, with flowers to litter, litter to flowers, and litter to dung being next, and then litter to roots, logs or carrion. Litter is again the largest overall source microhabitat. The most common transitions were to foliage and flowers. It thus seems that the litter environment presents ecological and evolutionary opportunities/challenges that facilitate entry of Staphyliniformia and Scarabaeiformia into ‘new’ and different ecological adaptive zones.

Molecular phylogeny, evolution and classification of the Hydrophilidae (Coleoptera)

The phylogeny and evolutionary history of the water scavenger beetles (Coleoptera: Hydrophilidae) are inferred from comprehensive analyses of DNA sequence data from the mitochondrial genes COI, COII and 16S and the nuclear genes 18S, 28S and arginine kinase. Bayesian and maximum parsimony analyses included 151 taxa, representing all subfamilies, tribes and subtribes that have ever been proposed in the family, as well as representatives of the hydrophiloid families Helophoridae, Hydrochidae, Spercheidae, Epimetopidae and Georissidae. The resulting well‐supported trees strongly disagree with prior classifications of the Hydrophilidae, suggesting that the smaller subfamilies (Horelophinae, Horelophopsinae and Sphaeridiinae) are derived from within the larger Hydrophilinae. The existing tribal classification is more compatible with our results, but many significant differences are evident. Here, we present a new classification of the Hydrophilidae comprising 6 subfamilies and 12 tribes. Each subfamily and tribe is reviewed in detail with (i) a morphological diagnosis, including known or putative morphological synapomorphies, (ii) its taxonomic circumscription, including genera not included in our analyses, and (iii) a review of its general biology and geographic distribution. A new identification key to subfamily and tribe based on adult morphology is also provided. The newly adopted classification requires the following taxonomic changes: the subfamily Hydrophilinae sensu n. is redefined to include only the tribes Amphiopini stat.n. (removed from the synonymy with the Chaetarthriini), Berosini, Laccobiini, Hydrophilini and Hydrobiusini (= Sperchopsini syn.n.); the subfamily Chaetarthriinae stat.n. is removed from synonymy with the Hydrophilinae and includes the tribes Chaetarthriini and Anacaenini (= Horelophinae syn.n.); the Acidocerinae stat.n. (= Horelophopsinae syn.n.) and Rygmodinae stat.n. (= Andotypini syn.n., Borborophorini syn.n. and Tormissini syn.n.) are elevated to subfamily rank; and the subfamily Enochrinae subfam.n. is established for the genus Enochrus and its relatives. The implications for the morphological evolution, ecological transitions and biogeography of the family are discussed.

Microhabitat and landscape influences on aquatic beetle assemblages in a cluster of temporary and permanent ponds

Aquatic beetles often have been regarded as mobile transients among water bodies, but recent studies suggest strong environmental influences on distribution and thus the potential for using beetles as bioindicators of habitat quality. We related aquatic beetle assemblage structure to environmental characteristics at 9 sites within a 0.5-km2 landscape in northern Delaware, USA. We sampled 6 temporary ponds (3 closed-canopy sites with short hydroperiods and 3 open-canopy sites with longer hydroperiods) and 3 permanent pond sites within a beaver pond. To evaluate microhabitats within ponds, we collected 6 shoreline and 6 deepwater samples at each site in early and late spring 2000 (n = 216), and classified samples according to 1 of 4 substrate types (dead leaves, Sphagnum, herbaceous vascular vegetation, and other substrate). Of the 46 species present in the samples, 5 were more abundant in temporary ponds, whereas 8 were more abundant at permanent sites. Similarly, 6 of 22 genera of larvae were more abundant in temporary ponds, whereas 7 were more abundant at permanent sites. We observed strong microhabitat affinities, with ∼85% of all individuals found along pond margins and ∼40% of all taxa associated with particular substrate types. Rates of species accrual relative to the number of individuals sampled increased late in the spring season, reflecting in part the timing of dispersal among ponds.

Larval Morphology of Meruidae (Coleoptera: Adephaga) and Its Phylogenetic Implications

ABSTRACT Meruidae, or comb-clawed cascade beetles, are a recently discovered monotypic family of Adephaga endemic to Venezuela. The larvae of Meruidae are described for the first time, based on material of Meru phyllisae Spangler & Steiner, 2005, collected together with adults in southern Venezuela. External morphological features, including chaetotaxy, are reported for the mature larva and an assessment made of the polarity of larval characters of phylogenetic utility in Adephaga. Larvae of Meruidae possess a mixture of primitive and derived character states, and they are unique within the Adephaga in that here the mandibles are asymmetrical, the respiratory system is comprised of only two pairs of spiracles (= oligopneustic), the claws are pectinate, and the abdominal sternite VIII is prolonged overlapping the abdominal sternite IX. A parsimony analysis based on 18 informative larval characteristics was conducted with the program PAUP*. The most parsimonious trees confirm Meruidae as a relatively basal lineage within the Dytiscoidea. Both Meru Spangler & Steiner and Noteridae are hypothesized to have diverged anterior to Amphizoidae, Aspidytidae, Hygrobiidae, and Dytiscidae.

The peril of dating beetles

Recently, McKenna et al., 2015 (MCK15 hereafter) investigated the higher level phylogenetic relationships of beetles (Insecta, Coleoptera) using the most comprehensive molecular dataset to date, and inferred the absolute ages of major groups using multiple fossil calibrations across the beetle tree of life. Based on the result of their dating analysis, beetles diverged from Strepsiptera in the Early Permian c. 278.33 Ma with a 95% credibility interval (95% CI) of 288.28 to 271.89 Ma, and the crown age of Coleoptera was estimated for the Late Permian c. 252.89 Ma (95% CI: 267.68 to 238.78 Ma), supporting the view that beetles originated before and survived through the End-Permian Mass Extinction that occurred c. 252 Ma (Shen et al., 2011). However, some of the age estimates found in MCK15 are in conflict with current knowledge of the beetle fossil record (e.g. Nikolajev & Ren, 2010; Pan et al., 2011, Prokin & Ren, 2011; Fikáček et al., 2012a; Wang et al., 2013, 2014; Cai et al., 2014b, 2015a; Kirejtshuk et al., 2014; Boucher et al., 2016) and with other recently published molecular age estimates for some major beetle clades (e.g. Zhang & Zhou, 2013; Ahrens et al., 2014; Bloom et al., 2014; Kergoat et al., 2014; Kim & Farrell, 2015; Bocák et al., 2016; Gunter et al., 2016). In some cases, the difference in age estimates is significant and might change our understanding of the mode and tempo of diversification dynamics of these groups. Based on a careful examination of the data and analyses performed in MCK15, we propose that the divergence time estimates which they found are likely to underestimate clade ages. We believe this is due to the subset of fossil Coleoptera that MCK15 selected as calibration points, as well as the methodological approach used in their analyses. To explore the impact of fossil selection on the age of Coleoptera, we derived an alternative set of fossil calibration points based on best-practice recommendations (e.g. Parham et al., 2012),

Clade Age and Diversification Rate Variation Explain Disparity in Species Richness among Water Scavenger Beetle (Hydrophilidae) Lineages

Explaining the disparity of species richness across the tree of life is one of the great challenges in evolutionary biology. Some lineages are exceptionally species rich, while others are relatively species poor. One explanation for heterogeneity among clade richness is that older clades are more species rich because they have had more time to accrue diversity than younger clades. Alternatively, disparity in species richness may be due to among-lineage diversification rate variation. Here we investigate diversification in water scavenger beetles (Hydrophilidae), which vary in species richness among major lineages by as much as 20 fold. Using a time-calibrated phylogeny and comparative methods, we test for a relationship between clade age and species richness and for shifts in diversification rate in hydrophilids. We detected a single diversification rate increase in Megasternini, a relatively young and species rich clade whose diversity might be explained by the stunning diversity of ecological niches occupied by this clade. We find that Amphiopini, an old clade, is significantly more species poor than expected, possibly due to its restricted geographic range. The remaining lineages show a correlation between species richness and clade age, suggesting that both clade age and variation in diversification rates explain the disparity in species richness in hydrophilids. We find little evidence that transitions between aquatic, semiaquatic, and terrestrial habitats are linked to shifts in diversification rates.

On the validity of habitat as a predictor of genetic structure in aquatic systems: a comparative study using California water beetles

Among freshwater organisms, water flow is frequently considered to be one of the most important environmental variables affecting life‐history traits such as dispersal abilities and therefore genetic structure. Recent studies have suggested that habitat type alone as defined by water flow is predictive of genetic population differentiation, while others have advocated against broad generalizations in favour of more conservative, species‐specific conclusions. If aquatic habitat type is predictive of population differentiation, then one would expect sympatric taxa that occupy the same aquatic habitat to converge on a similar genetic structure. We tested this prediction by examining the haplotype diversity, phylogeographical concordance, population connectivity and population isolation of three lotic water beetle species in southern California: Anacaena signaticollis, Eubrianax edwardsii and Stictotarsus striatellus. In addition to coarse habitat and geography, we also controlled for the potentially confounding factors of range size, method of dispersal and clade independence. Together, the species spanned extremes of genetic and phylogeographical structure in all measures examined, suggesting that a coarse dichotomy of aquatic habitat type is not predictive of genetic structure. While there is little question that water flow plays a major role in shaping the life‐history traits of freshwater organisms, it is perilous to confer predictive properties to an artificially simplistic dichotomy or use it as a surrogate for other unmeasured variables.

Phylogeny, evolution and classification of the giant water scavenger beetles (Coleoptera: Hydrophilidae: Hydrophilini: Hydrophilina)

The hydrophiline subtribe Hydrophilina is composed of nearly 200 described species, including all known water scavenger beetles over 15 mm in length. Found in all biogeographic regions, the lineage is the most recognizable group in the family due to its large size and presence of a sternal keel. A phylogenetic analysis of Hydrophilina based on 80 adult morphological characters supports the reciprocal monophyly of most genera, including Tropisternus Solier, Sternolophus Solier, Hydrophilus Geoffroy, and Hydrobiomorpha (s. str.) Blackburn. The monophyly of Hydrochara Berthold was not resolved. The subgenus Brownephilus Mouchamps of the genus Hydrobiomorpha is elevated to generic rank and suggested to subtend (Hydrophilus+ Hydrobiomorpha (s. str.)). A newly discovered taxon from Venezuela, Protistolophus spangleri gen. et sp. nov., is described and resolved as the earliest diverging lineage of the Hydrophilina. A revised generic classification of the Hydrophilina is proposed, including a key and revised diagnoses for each genus. The evolution of giantism and complex secondary sexual characters are discussed in the context of the newly developed phylogenetic hypothesis.

Evolution of Pacific Rim diving beetles sheds light on Amphi‐Pacific biogeography

The origin of biodiversity in the Neotropics predominantly stems either from Gondwana breakup or late dispersal events from the Nearctic region. Here, we investigate the biogeography of a diving beetle Glade whose distribution encompasses parts of the Oriental region, the Indo-Australian archipelago (IAA) and the Neotropics. We reconstructed a dated molecular phylogeny, inferred diversification dynamics and estimated ancestral areas under different biogeographic assumptions. For the Oriental region and the IAA, we reveal repeated and complex colonization patterns out of Australia, across the major biogeographic lines in the region (e.g. Wallaces Line). The timing of colonization events across the IAA broadly coincides with the proposed timing of the formation of major geographic features in the region. Our phylogenetic hypothesis recovers Neotropical species nested in two derived clades. We recover an origin of the group in the early Eocene about 55 million yr ago, long after the break-up of Gondwana initiated, but before a complete separation of Australia, Antarctica and the Neotropics. When allowing an old Gondwanan ancestor, we reconstruct an intricate pattern of Gondwanan vicariance and trans-Pacific long-distance dispersal from Australia toward the Neotropics. When restricting the ancestral range to more plausible geological area combinations in the Eocene, we infer an Australian origin with two trans-Pacific long-distance dispersal events toward the Neotropics. Our results support on one hand a potential Gondwanan signature associated with regional extinctions in the Cenozoic and with Antarctica serving as a link between Australia and the Neotropics. On the other hand, they also support a trans-Pacific dispersal of these beetles toward the Andean coast in the Oligocene.

Ultraconserved elements show utility in phylogenetic inference of Adephaga (Coleoptera) and suggest paraphyly of ‘Hydradephega’

The beetle suborder Adephaga has been the subject of many phylogenetic reconstructions utilizing a variety of data sources and inference methods. However, no strong consensus has yet emerged on the relationships among major adephagan lineages. Ultraconserved elements (UCEs) have proved useful for inferring difficult or unresolved phylogenies at varying timescales in vertebrates, arachnids and Hymenoptera. Recently, a UCE bait set was developed for Coleoptera using polyphagan genomes and a member of the order Strepsiptera as an outgroup. Here, we examine the utility of UCEs for reconstructing the phylogeny of adephagan families, in the first in vitro application a UCE bait set in Coleoptera. Our final dataset included 305 UCE loci for 18 representatives of all adephagan families except Aspidytidae, and two polyphagan outgroups, with a total concatenated length of 83 547 bp. We inferred trees using maximum likelihood analyses of the concatenated UCE alignment and coalescent species tree methods (astral ii, ASTRID, svdquartets). Although the coalescent species tree methods had poor resolution and weak support, concatenated analyses produced well‐resolved, highly supported trees. Hydradephaga was recovered as paraphyletic, with Gyrinidae sister to Geadephaga and all other adephagans. Haliplidae was recovered as sister to Dytiscoidea, with Hygrobiidae and Amphizoidae successive sisters to Dytiscidae. Finally, Noteridae was recovered as monophyletic and sister to Meruidae. Given the success of UCE data for resolving phylogenetic relationships within Adephaga, we suggest the potential for further resolution of relationships within Adephaga using UCEs with improved taxon sampling, and by developing Adephaga‐specific probes.